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Acta Agronomica Sinica ›› 2024, Vol. 50 ›› Issue (12): 2971-2983.doi: 10.3724/SP.J.1006.2024.44071

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Mechanism of reduced insecticidal protein expression in Bt cotton under low-iron stress based on transcriptome analysis

WANG Yong-Hui(), HE Jiang, ZHANG Xiang-Xiang, LOU Xiang-Di, GAO Jing, SUN Yan-Ru, CAO Ting, SHI Yang   

  1. Institute of Agricultural Sciences of Jiangsu Coastal Area / Observation and Experimental Station of Saline land of Costal Area, Ministry of Agriculture and Rural Affairs, Yancheng 224001, Jiangsu, China
  • Received:2024-04-26 Accepted:2024-08-15 Online:2024-12-12 Published:2024-09-02
  • Contact: *E-mail: huiyw2008@163.com
  • Supported by:
    National Natural Science Foundation of China(31501267);Jiangsu Agriculture Science and Technology Innovation Fund [(CX(20)2065)

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Abstract:

To provide a theoretical basis for the safety of insecticidal efficiency in Bt cotton, this study investigated the effects of low iron on Bt insecticidal protein content and the physiological and molecular mechanisms in Bt cotton. Transgenic Bt cotton cultivar Zhongmian 50 was grown under low iron (LI, 0.1 μmol L-1 Fe(II)-EDTA) and normal iron (CK, 20.0 μmol L-1 Fe(II)-EDTA) conditions in hydroponic culture to assess the impact of low iron stress on Bt insecticidal protein content, activities of nitrogen metabolism-related enzymes, and substances in cotton seedlings. Differentially expressed genes (DEGs) were screened, and their relative expression patterns were analyzed by high-throughput sequencing, with results verified by qRT-PCR. The results showed that, compared with the control, the insecticidal protein contents significantly decreased under low iron conditions, with a more pronounced reduction in roots than in leaves. Iron deficiency decreased NH4+-N and NO3--N levels in leaves and reduced soluble protein and nitrogen contents in both roots and leaves. Significant reductions in the activities of nitrate reductase (NR), nitrite reductase (NiR), and glutamine synthetase (GS) were observed when Bt insecticidal protein contents in roots and leaves were significantly reduced. High-throughput sequencing identified 11,661 DEGs in roots and 8972 in leaves, with 1652 genes down-regulated in both organs. GO annotation revealed that the functions of the differential genes in two organs were mainly concentrated in response to stimulus, cell wall, plasma membrane, binding, and catalytic activity. KEGG enrichment analysis demonstrated significant changes in phenylpropanoid biosynthesis, phenylalanine metabolism, cysteine and methionine metabolism, plant hormone signal transduction, zeatin biosynthesis, nitrogen metabolism, starch and sucrose metabolism, alanine, aspartate and glutamate metabolism, and tyrosine metabolism in both roots and leaves. Genes coding for NR, NiR1, and GLT1 related to the nitrogen reduction and assimilation pathway were significantly down-regulated under iron deficiency treatment. Therefore, low iron stress inhibits the transcription levels of genes related to nitrogen metabolism in Bt cotton, weakens the physiological activities of nitrogen metabolism, and subsequently reduces Bt insecticidal protein.

Key words: Bt cotton, insecticidal protein, low iron, transcriptome

Table 1

Primers for qRT-PCR"

基因名称
Gene name		 正向引物
Forward sequence (5′-3′)		 反向引物
Reverse sequence (5′-3′)		 基因 ID
Gene ID
ACT14 CTGGAGACTGCCAAGAGCAGCT CCGGGCAACGGAATCTCTCAGC
NR GAGCATATCCCGGTGGGTTC GCTGCACAGCGAACTGAATC Gh_D02G0815
NiR1 GGGGCAGACATATTCTTGGGA AGCTCCAAAGTGTTCCACCA Gh_A13G0352
GS1.1 CAATTCGTGTTGGGCGAGAC CAAACATGGGCTTCCCCTCA Gh_A13G0512
GLT1 CGGAGGCTTGTGCTGAGTAT TCTGTACAGTGTGGGGCAAG Gh_D12G2422

Fig. 1

Effects of low iron stress on dry weight and iron content in the roots and leaves of Bt cotton A: effects of low iron stress on dry weight in the roots and leaves of Bt cotton; B: effects of low iron stress on iron content in the roots and leaves of Bt cotton. CK: 20 μmol L-1 Fe (II)-EDTA; LI: 0.1 μmol L-1 Fe (II)-EDTA. Different lowercase letters represent significant difference among treatments at the P < 0.05."

Fig. 2

Effects of low iron stress on insecticidal protein content in the roots and leaves of Bt cotton Treatments are the same as those given in Fig. 1. Different lowercase letters represent significant difference among treatments at the P < 0.05."

Table 2

Effects of low iron stress on nitrate reductase (NR), nitrite reductase (NiR), glutamine synthetase (GS) and glutamate synthase (GOGAT) activities in the roots and leaves of Bt cotton"

器官/处理
Organ/ treatment		 硝酸还原酶活性
Nitrate reductase activities
(μmol g-1 h-1)		 亚硝酸还原酶活性
Nitrite reductase activities
(μmol g-1 h-1)		 谷氨酰胺合成酶活性
Glutamine synthetase
activities
(ΔA g-1 h-1)		 谷氨酸合成酶活性
Glutamate synthase activities
(µmol g-1 min-1)
根系Root
CK 3.35 a 7.85 a 0.77 a 0.76 a
LI 2.79 b 6.97 b 0.34 b 0.44 b
叶片Leaf
CK 5.13 a 10.82 a 0.86 a 1.02 a
LI 3.54 b 9.03 b 0.83 a 0.81 b

Table 3

Effects of low iron stress on NH4+-N, NO3--N, soluble protein, and N content in the roots and leaves of Bt cotton"

器官/处理
Organ/ treatment		 铵态氮
NH4+-N
(μg g-1 FW)		 硝态氮
NO3--N
(μmol g-1 FW)		 可溶性蛋白含量
Soluble protein content
(mg g-1 FW)		 全氮含量
N content
(mg g-1 DW)
根系Root
CK 6.6 a 13.4 a 12.7 a 41.4 a
LI 6.8 a 14.1 a 9.3 b 35.8 b
叶片Leaf
CK 13.2 a 26.4 a 21.3 a 57.1 a
LI 10.3 b 17.6 b 17.8 b 51.8 b

Table 4

Statistical analysis of transcriptome sequencing basic data"

样品
Sample		 原始数据
Raw reads		 有效数据
Clean reads		 总映射率
Total mapped rate (%)		 唯一映射率
Uniquely mapped rate (%)		 Q30
(%)		 GC 含量
GC content (%)
RCK_1 46,179,118 45,290,042 98.13 93.01 94.27 42.77
RCK_2 47,909,866 46,989,512 98.17 93.05 94.05 42.76
RCK_3 46,776,936 45,955,806 98.20 93.17 94.41 42.73
RLI_1 36,534,072 35,735,176 96.03 92.59 94.18 43.28
RLI_2 42,611,888 41,690,972 96.02 92.72 94.18 43.29
RID_3 36,994,328 36,155,932 95.98 92.77 94.03 43.30
LCK_1 47,984,028 47,017,502 98.50 91.19 94.25 44.13
LCK_2 54,041,314 53,158,296 98.55 92.01 94.24 44.13
LCK_3 45,829,824 44,978,082 98.55 91.28 94.13 44.15
LLI_1 37,090,636 36,270,280 98.48 91.46 94.09 43.65
LLI_2 46,722,582 45,791,778 98.49 91.67 94.26 43.65
LLI_3 50,516,840 49,554,758 98.46 91.53 94.34 43.62

Fig. 3

Differentially expressed genes (DEGs) under low iron stress A: numbers of up-regulate and down-regulate genes in each sample; B: Venn diagram of differentially expressed genes. Abbreviations are the same as those given in Table 4."

Table 5

GO annotation of differentially expressed genes (DEGs)"

GO号
GO ID		 GO功能
GO function		 总基因数目
Total numbers		 RCK vs RLI
差异基因数目
DEG numbers in
RCK vs RLI		 LCK vs LLI
差异基因数目
DEG numbers in
LCK vs LLI		 GO类别
Category
GO:0071555 细胞壁组织
Cell wall organization		 1433 349 319 BP
GO:0071554 细胞壁组织或生物发生
Cell wall organization or biogenesis		 1904 447 398 BP
GO:0050896 刺激反应
Response to stimulus		 15,817 3040 2434 BP
GO:0009725 对激素的反应
Response to hormone		 5317 1134 885 BP
GO:0055072 铁离子平衡
Iron ion homeostasis		 148 62 50 BP
GO:0005576 胞外区
Extracellular region		 2833 733 588 CC
GO:0071944 细胞外围
Cell periphery		 9137 1803 1528 CC
GO:0030312 外部封装结构
External encapsulating structure		 1816 466 387 CC
GO:0005618 细胞壁
Cell wall		 1775 453 375 CC
GO:0005886 质膜
Plasma membrane		 7785 1470 1263 CC
GO:0031226 质膜的内在成分
Intrinsic component of plasma membrane		 922 237 224 CC
GO:0031224 膜的内在成分
Intrinsic component of membrane		 10,103 1841 1646 CC
GO:0031225 膜锚定组件
Anchored component of membrane		 412 122 125 CC
GO:0003700 DNA结合转录因子活性
DNA-binding transcription factor activity		 3821 899 644 MF
GO:0016491 氧化还原酶活性
Oxidoreductase activity		 3512 827 671 MF
GO:0046906 四吡咯结合
Tetrapyrrole binding		 863 246 194 MF
GO:0020037 血红素结合
Heme binding		 736 236 156 MF

Fig. 4

Scatter diagram of KEGG pathway enrichment Abbreviations are the same as those given in Table 4."

Fig. 5

Heatmaps of differentially expressed genes (DEGs) related NRT and AMT family Abbreviations are the same as those given in Table 4."

Table 6

Relative expression profiles of differentially expressed genes (DEGs) in the nitrogen metabolism pathway"

基因ID
Gene ID		 基因功能注释
Gene function annotation		 调控Regulation 基因名称
Gene name
RCK vs RLI LCK vs LLI
Gh_D02G0815 硝酸还原酶[NADH]
Nitrate reductase [NADH]		 ↓ ↓ NR
Gh_A02G0769 硝酸还原酶[NADH]
Nitrate reductase [NADH]		 ↓ ↓ NR
Gh_A01G1586 硝酸还原酶[NADH]
Nitrate reductase [NADH]		 -- ↓ NR
Gh_D01G1872 硝酸还原酶[NADH]
Nitrate reductase [NADH]		 ↑ ↓ NR
Gh_A13G0352 铁氧还蛋白-亚硝酸盐还原酶, 叶绿体 ↓ ↓ NiR1
Ferredoxin-nitrite reductase, chloroplastic
Gh_D07G1773 谷氨酰胺合成酶, 胞质同工酶1 ↑ ↑ GS1;1
Glutamine synthetase, cytosolic isozyme 1
Gh_A13G0512 谷氨酰胺合成酶, 胞质同工酶1 ↑ ↑ GS1;1
Glutamine synthetase, cytosolic isozyme 1
Gh_D13G0620 谷氨酰胺合成酶, 胞质同工酶1 -- ↑ GS1;1
Glutamine synthetase, cytosolic isozyme 1
Gh_D11G3479 谷氨酰胺合成酶, 结节同工酶 ↑ ↓ GS
Glutamine synthetase, nodule isozyme
Gh_D09G1909 谷氨酰胺合成酶, 叶同工酶, 叶绿体 ↓ -- GS
Glutamine synthetase, leaf isozyme, chloroplastic
Gh_A09G1788 谷氨酰胺合成酶, 叶同工酶, 叶绿体 ↓ -- GS
Glutamine synthetase, leaf isozyme, chloroplastic
Gh_D12G2422 谷氨酸合成酶 1 [NADH], 叶绿体 ↓ ↓ GLT1
Glutamate synthase 1 [NADH], chloroplastic
Gh_A12G2272 谷氨酸合成酶 1 [NADH], 叶绿体 ↓ -- GLT1
Glutamate synthase 1 [NADH], chloroplastic

Fig. 6

Verification of the differentially expressed genes by qRT-PCR"

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